Metabolomic Profiles of Multidrug-Resistant Salmonella Typhimurium from Humans, Bovine, and Porcine Hosts
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Isolate Collection, Screening, Identification, and Growth
2.2. Integron and AMR Testing
2.3. Isolate Growth and Extraction for Proteomic and Metabolomics Profiling
2.4. Metabolomic Profiling by UPLC- and GC–MS
2.5. Statistical Analysis (MetaboAnalyst 4.0)
3. Results
3.1. AMR Patterns and Integrons
3.2. Metabolite Expression by Drug Treatment and Host Species
3.3. Metabolite Expression and Matched Metabolic Pathways
3.4. Univariate Analysis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Drug Panel | MIC |
---|---|
Ampicillin | 32 µg/mL |
Chloramphenicol | 32 µg/mL |
Streptomycin | 64 µg/mL |
Sulfisoxazole | 512 µg/mL |
Tetracycline | 16 µg/mL |
All Hosts | Bovine | Swine | Human | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Metabolic Pathway | Impact | p-Value | FDR | Metabolite | Fold Change (FD/ND) | p-Value | FDR | Fold Change (FD/ND) | p-Value | FDR | Fold Change (FD/ND) | p-Value | FDR | Fold Change (FD/ND) | p-Value | FDR |
Aminoacyl-tRNA biosynthesis | 0.2 | 1.93 × 10−7 | 1.66 × 10−5 | Phenylalanine | 0.565 | 0.0000581 | 0.00043499 | 0.433 | 0.0021645 | 0.0096991 | 0.737 | 0.535 | ||||
Cysteine | 1.515 | 0.0096309 | 0.023444 | 0.118 | 0.0021645 | 0.0096991 | 0.228 | 0.0021645 | 0.022605 | 1.400 | ||||||
Glycine | 1.858 | 0.00000394 | 0.0000655 | 2.003 | 0.0021645 | 0.0096991 | 1.812 | 1.723 | ||||||||
Aspartate | 3.077 | 3.06 × 10−8 | 0.00000283 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 2.178 | ||||||
Serine | 2.837 | 8.22 × 10−8 | 0.00000426 | 4.469 | 0.0021645 | 0.0096991 | 1.755 | 0.0021645 | 0.022605 | 2.240 | ||||||
Methionine | 0.594 | 0.020464 | 0.042605 | 0.498 | 0.0021645 | 0.0096991 | 0.588 | 0.708 | ||||||||
Valine | 0.675 | 0.0064022 | 0.017165 | 0.391 | 0.0021645 | 0.0096991 | 0.925 | 0.782 | ||||||||
Alanine | 2.065 | 3.06 × 10−8 | 0.00000283 | 2.149 | 0.0021645 | 0.0096991 | 2.240 | 0.0021645 | 0.022605 | 1.910 | ||||||
Leucine | 0.087 | 0.0023492 | 0.0080271 | 0.106 | 0.015152 | 0.041482 | 0.063 | 0.0021645 | 0.022605 | 0.116 | ||||||
Threonine | 2.233 | 2.2 × 10−10 | 0.000000285 | 2.065 | 0.0021645 | 0.0096991 | 3.156 | 0.0021645 | 0.022605 | 1.834 | ||||||
Tryptophan | 2.143 | 0.0000164 | 0.00017127 | 1.789 | 0.0021645 | 0.0096991 | 2.671 | 1.647 | ||||||||
Tyrosine | 2.183 | 1.48 × 10−8 | 0.00000212 | 2.932 | 0.0021645 | 0.0096991 | 2.054 | 0.0021645 | 0.022605 | 1.959 | ||||||
Proline | 2.150 | 0.00075777 | 0.0033152 | 1.153 | 3.432 | 2.041 | ||||||||||
Glutamate | 0.321 | 0.0000239 | 0.00021944 | 0.353 | 0.497 | 0.243 | ||||||||||
Pantothenate and CoA biosynthesis | 0.144 | 0.00304 | 0.10686 | Pantothenate | 0.414 | 0.000000 | 0.000005 | 0.440 | 0.0021645 | 0.0096991 | 0.389 | 0.0021645 | 0.022605 | 0.429 | ||
Valine | 0.675 | 0.006402 | 0.017165 | 0.391 | 0.0021645 | 0.0096991 | 0.925 | 0.782 | ||||||||
Aspartate | 3.077 | 0.000000 | 0.000003 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 1.300 | ||||||
Cysteine | 1.515 | 0.009631 | 0.023444 | 0.118 | 0.0021645 | 0.0096991 | 0.228 | 0.0021645 | 0.022605 | 1.400 | ||||||
Pyruvate | 0.458 | 0.002642 | 0.008841 | 0.382 | 0.008658 | 0.026381 | 1.570 | 0.0021645 | 0.022605 | 0.394 | ||||||
Uracil | 1.477 | 0.020464 | 0.042605 | 0.977 | 1.848 | 1.474 | ||||||||||
Glycine, serine, and threonine metabolism | 0.456 | 0.00373 | 0.10686 | Serine | 2.837 | 0.000000 | 0.000004 | 4.469 | 0.0021645 | 0.0096991 | 1.755 | 0.0021645 | 0.022605 | 2.240 | ||
Glycine | 1.858 | 0.000004 | 0.000066 | 2.003 | 0.0021645 | 0.0096991 | 1.812 | 1.723 | ||||||||
Aspartate | 3.077 | 0.000000 | 0.000003 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 1.300 | ||||||
Glycerate | 1.691 | 0.000503 | 0.002423 | 0.631 | 0.008658 | 0.026381 | 2.225 | 2.473 | ||||||||
Threonine | 2.233 | 0.000000 | 0.000000 | 2.065 | 0.0021645 | 0.0096991 | 3.156 | 0.0021645 | 0.022605 | 1.834 | ||||||
Pyruvate | 0.458 | 0.002642 | 0.008841 | 0.382 | 0.008658 | 0.026381 | 1.570 | 0.0021645 | 0.022605 | 0.394 | ||||||
Tryptophan | 2.143 | 0.000016 | 0.000171 | 1.789 | 0.0021645 | 0.0096991 | 2.671 | 1.647 | ||||||||
Glutathione metabolism | 0.118 | 0.01061 | 0.2144 | Glycine | 1.858 | 0.000004 | 0.000066 | 2.003 | 0.0021645 | 0.0096991 | 1.812 | 1.723 | ||||
Cysteine | 1.515 | 0.009631 | 0.023444 | 0.118 | 0.0021645 | 0.0096991 | 0.228 | 0.0021645 | 0.022605 | 1.400 | ||||||
Pyroglutamic Acid | 0.679 | 0.005177 | 0.014605 | 0.613 | 0.748 | 0.693 | ||||||||||
Glutamate | 0.321 | 0.000024 | 0.000219 | 0.353 | 0.497 | 0.243 | ||||||||||
Nicotinate and Nicotinamide metabolism | 0.066 | 0.0125 | 0.2144 | Aspartate | 3.077 | 0.000000 | 0.000003 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 1.300 | ||
Glycerone phosphate | 0.582 | 0.000001 | 0.000027 | 0.644 | 0.004329 | 0.016886 | 0.579 | 0.0021645 | 0.022605 | 0.536 | ||||||
Nicotinamide | 1.858 | 0.000245 | 0.001366 | 1.505 | 1.666 | 2.495 | ||||||||||
Nicotinate | 1.435 | 0.000007 | 0.000098 | 1.587 | 0.008658 | 0.026381 | 1.455 | 1.832 | ||||||||
Glyoxylate and dicarboxylate metabolism | 0.055 | 0.0269 | 0.38631 | Citrate | 7.934 | 0.000024 | 0.000219 | 2.799 | 20.017 | 6.503 | ||||||
Glycerate | 1.691 | 0.000503 | 0.002423 | 0.631 | 0.008658 | 0.026381 | 2.225 | 2.473 | ||||||||
Glycine | 1.858 | 0.000004 | 0.000066 | 2.003 | 0.0021645 | 0.0096991 | 1.812 | 1.723 | ||||||||
Glutamate | 0.321 | 0.000024 | 0.000219 | 0.353 | 0.497 | 0.243 | ||||||||||
Serine | 2.837 | 0.000000 | 0.000004 | 4.469 | 0.0021645 | 0.0096991 | 1.755 | 0.0021645 | 0.022605 | 2.240 | ||||||
Pyruvate | 0.458 | 0.002642 | 0.008841 | 0.382 | 0.008658 | 0.026381 | 1.570 | 0.0021645 | 0.022605 | 0.394 | ||||||
beta-Alanine Metabolism | 0 | 0.0458 | 0.43434 | Aspartate | 3.077 | 0.000000 | 0.000003 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 1.300 | ||
Pantothenate | 0.414 | 0.000000 | 0.000005 | 0.440 | 0.0021645 | 0.0096991 | 0.389 | 0.0021645 | 0.022605 | 0.429 | ||||||
Uracil | 1.477 | 0.020464 | 0.042605 | 0.977 | 1.848 | 1.474 | ||||||||||
Valine, leucine, and isoleucine biosynthesis | 0.107 | 0.0475 | 0.43434 | Threonine | 2.233 | 0.000000 | 0.000000 | 2.065 | 0.0021645 | 0.0096991 | 3.156 | 0.0021645 | 0.022605 | 1.834 | ||
Leucine | 0.087 | 0.002349 | 0.008027 | 0.106 | 0.015152 | 0.041482 | 0.063 | 0.0021645 | 0.022605 | 0.116 | ||||||
Pyruvate | 0.458 | 0.002642 | 0.008841 | 0.382 | 0.008658 | 0.026381 | 1.570 | 0.0021645 | 0.022605 | 0.394 | ||||||
Valine | 0.675 | 0.006402 | 0.017165 | 0.391 | 0.0021645 | 0.0096991 | 0.925 | 0.782 | ||||||||
Alanine, aspartate and glutamate metabolism | 0.45 | 0.0475 | 0.43434 | Aspartate | 3.077 | 0.000000 | 0.000003 | 3.174 | 0.0021645 | 0.0096991 | 3.883 | 0.0021645 | 0.022605 | 1.300 | ||
Alanine | 2.065 | 0.000000 | 0.000003 | 2.149 | 0.0021645 | 0.0096991 | 2.240 | 0.0021645 | 0.022605 | 1.910 | ||||||
Glutamate | 0.321 | 0.000024 | 0.000219 | 0.353 | 0.497 | 0.243 | ||||||||||
Pyruvate | 0.458 | 0.002642 | 0.008841 | 0.382 | 0.008658 | 0.026381 | 1.570 | 0.0021645 | 0.022605 | 0.394 |
Metabolite | p-Value | FDR |
---|---|---|
2-Piperidinecarboxylic_acid_1MEOX_2TMS | 0.00958 | 0.04464 |
Adenine_1TMS | 0.00275 | 0.02104 |
Alanine, N-3-indolylacetyl | 0.00002 | 0.00135 |
Aspartic acid, N-3-indolylacetyl | 0.00000 | 0.00032 |
Butanoic acid,_3-hydroxy-0.2 | 0.00064 | 0.00847 |
Butanoic_acid, 4-hydroxy-_2TMS | 0.00035 | 0.00576 |
Cinnamic_acid, 2-hydroxy-, trans- | 0.000003 | 0.00040 |
Cohibin_A.1 | 0.00374 | 0.02508 |
Coixenolide_2 | 0.00869 | 0.04154 |
Coixenolide_4 | 0.00561 | 0.03144 |
Cysteamine_3TMS | 0.00531 | 0.03071 |
Cysteine_3TMS | 0.01144 | 0.04989 |
Glycerol-3-phosphate_4TMS.2 | 0.00118 | 0.01276 |
Glycine | 0.00004 | 0.00173 |
Guanosine | 0.00001 | 0.00088 |
Guanosine,_2′-deoxy-_4TMS.1 | 0.00027 | 0.00504 |
Guanosine_4TMS coeluting_with_Guanosine_5TMS | 0.00261 | 0.02063 |
Iminodiacetic_acid_3TMS | 0.00185 | 0.01715 |
Isoleucine_2TMS | 0.00071 | 0.00914 |
Lactose | 0.00001 | 0.00065 |
Leucine | 0.00032 | 0.00541 |
Leucine,_cyclo- | 0.00352 | 0.02428 |
Leucine_2TMS | 0.00051 | 0.00704 |
Levulinic_acid | 0.00057 | 0.00760 |
Luteolin | 0.00474 | 0.02871 |
Naringenin | 0.00066 | 0.00867 |
Oxamide_3TMS | 0.00017 | 0.00383 |
Pantothenic_acid,_D-_3TMS | 0.00799 | 0.04009 |
Phenylalanine_2TMS | 0.00003 | 0.00147 |
Phosphomycin | 0.000000008 | 0.00001 |
Pinitol,_D-_5TMS | 0.00363 | 0.02488 |
Putrescine_4TMS | 0.00224 | 0.01912 |
Pyridine | 0.00443 | 0.02729 |
Pyridoxamine | 0.00859 | 0.04136 |
Pyroglutamic_acid_2TMS | 0.00976 | 0.04528 |
Quercetin | 0.00003 | 0.00147 |
Serine | 0.00000003 | 0.00001 |
Thiamine | 0.00004 | 0.00173 |
Threitol,_dithio- | 0.00166 | 0.01589 |
Thymidine-5′-monophosphoric-acid-3TMS | 0.00020 | 0.00426 |
Tryptophan_3TMS | 0.00007 | 0.00249 |
Tyrosine,_2-iodo- | 0.000000017 | 0.00001 |
Tyrosine_3TMS | 0.00001 | 0.00094 |
Uric_acid | 0.00017 | 0.00383 |
Valine_2TMS | 0.00008 | 0.00280 |
Xanthine_3TMS | 0.00772 | 0.03903 |
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Overton, J.M.; Linke, L.; Magnuson, R.; Broeckling, C.D.; Rao, S. Metabolomic Profiles of Multidrug-Resistant Salmonella Typhimurium from Humans, Bovine, and Porcine Hosts. Animals 2022, 12, 1518. https://doi.org/10.3390/ani12121518
Overton JM, Linke L, Magnuson R, Broeckling CD, Rao S. Metabolomic Profiles of Multidrug-Resistant Salmonella Typhimurium from Humans, Bovine, and Porcine Hosts. Animals. 2022; 12(12):1518. https://doi.org/10.3390/ani12121518
Chicago/Turabian StyleOverton, Jessie M., Lyndsey Linke, Roberta Magnuson, Corey D. Broeckling, and Sangeeta Rao. 2022. "Metabolomic Profiles of Multidrug-Resistant Salmonella Typhimurium from Humans, Bovine, and Porcine Hosts" Animals 12, no. 12: 1518. https://doi.org/10.3390/ani12121518